The Fungal Apocalypse, Permo-Triassic Edition

There is something curious about the sedimentary rocks laid down around the world 250 million years ago, at the height of Earth's greatest extinction: they are often riddled with filaments, and no one is sure what they are. Nothing like them has been found in rocks before or since.

What seems apparent, and what everyone seems to agree on, is that they were once alive. Chemical signatures left in the rock by the fossils tell us this. But their appearance -- darkened branching filaments divided into cells up to 24 units long -- also seems very, well, lifey. What few agree on is their identity. Were they algae, thriving in ponds and swamps during some great deluge? Or were they wood-decay fungi feasting on the corpses of climate-felled conifer forests? Both have long been suggested, but here, the biochemical evidence is ambiguous. Whatever they were, something very strange was going on.

The Permo-Triassic Extinction, or Great Dying, that produced the rocks filled with these filaments seems to have been brought on by a massive slow-motion volcanic eruption in what is now Siberia 250 million years ago. According to the majority opinion, vast oozing plains of lava emitted catastrophic quantities of carbon dioxide and methane, poisoning the air for life. Other scenarios have been conjured involving ozone depletion, acidification, or the ever-popular asteroid impact1. Whatever the scenario, the result was staggering extinctions. About 90% of ocean life and 75% of land life vanished. Forests died. Soils eroded. General chaos ensued.

And somehow, something that made chains of little, brown barrel-shaped cells managed to make a, well, killing in the process.

It should be said that these fossils -- generally called Reduviasporonites -- bear a variety of appearances, and may represent several species (here is a nice gallery of their variety -- click "Galleries" at left). The filaments didn't resemble the active filaments (or hyphae -- high-fee) of known fungi, which are generally tubular and unpigmented. That led some to discount the fungal hypothesis. The key insight, it turned out, was that these were not normal fungal hyphae at all. They were something much more sinister.

A trio of scientists from Utrecht University, Imperial College, and the University of California-Berkeley recently noted that at least some Reduviasporonites from classic Permo-Triassic boundary rock in the Dolomites of northern Italy bear a striking resemblance to a pathogenic fungus: Rhizoctonia. And if this is the case, it raises a more ghoulish possibility: What if the fossil filaments are remnants of an orgy of fungal destruction, as pathogenic fungi feasted on helpless, dying trees in a noxious atmosphere lit from afar by endless plains of erupting lava? Interesting times, as they say.

If we're going by appearance (which they are), you can judge for yourself. Here is living Rhizoctonia solani:

Living Rhizoctonia solani, image courtesy Lane Tredway, copyright of The American Phytopathological Society. Used with permission; click image for link.

Compare with image at top. Uncanny, no?

And for comparison, here are some images (and also here) of two of the genera of the Zygnemataceae, the group of algae generally considered the other chief suspect (I am not certain these are the genera Reduviapsoronites are considered to be most like, but they were the genera with photographs available on the internet). Interestingly, these genera have stunningly beautiful star-shaped and spiral chloroplasts, the little green structures where plant cells make sugar from light. Yet to the naked eye, you would know them as pond scum.

Modern Rhizoctonia are interesting beasts. They are really an amalgam ("form group") of species united by their structure and M.O. When hyphae are young, they branch at almost perfect right angles. When mature, they make thickened, barrel-shaped short cells, as you can see at left, and the whole thing (mycelium, or my-seal-ee-um) is pigmented with the same stuff that darkens human skin.

Whether young or old, Rhizoctonia reproduce virtually without spores. For many years they were called "sterile fungi" by scientists because they were thought to never produce asexual spores called conidia (most fungi pump them out like they're going out of style). Now we know some do so very rarely. Spores produced by sexual reproduction (aka meiosis) are rare too. Instead, they seem to reproduce by breaking into pieces that wash or blow away.

Although this is all interesting (to bionerds like myself, anyway), these sterile, tough fungi are notorious for a different reason: they are tenacious plant pathogens. Rhizoctonia are known for producing a variety of nasty diseases on vegetables, flowers, shrubs, and trees -- from wilting newly sprouted seedlings to eating holes in the stems of grown plants in a botanical version of flesh-eating bacteria (these would be, of course, flesh-eating fungi). Root and stem rots are their specialties, and they especially like attacking anything in or near the soil, their base of operations.

Lots of seemingly unrelated things have evolved into this niche of sterile, plant pathogenic mycelium2. Some of them fall into the huge group of fungi called ascomycetes that make their sexual spores in sacs; others are basidiomycetes that make their sexual spores on the outside of club-shaped cells (one of them, Rhizoctonia leguminicola produces a wonderfully-named chemical in clover called slaframine, or "slobber factor" because it causes livestock who eat the clover it to drooluncontrollably).

They were once all called Rhizoctonia, but since only genetically related things can share names in biological nomenclature, scientists are busy sorting and renaming them. Still, that tells you it's a pretty popular niche, and convergent evolution -- when genetically unrelated creatures evolve to look and behave similarly, like whales and fish, or hummingbirds and insects(in my opinion) -- has been rife in it. We'll get back to this momentarily.

The alga Zygnema, pond scum (literally) and namesake of the Zygnemataceae, the other group Reduviasporonites has been suggested to resemble. Note the star-shaped chloroplasts. Creative Commons Bob Blaylock; Click image for license and link.

When Rhizoctonia is facing hard times, it makes disks of hardened, fortified mycelium called sclerotia by twisting chains of its dark, squat resting cells together. They pack the thing full of fats and sugars -- the fungal version of stocking your fallout-shelter with pallets of Dinty Moore -- and darken the cell walls for UV protection. Then they darken the lights, put on fuzzy slippers and a movie, and wait.

Lots of other fungi make sclerotia too. You can find them in many places if you rake aside the leaf or needle litter. Just below the duff, you'll find hard little structures sitting at the soil line. Sometimes they're quite colorful. These hardened resting structures are a major way fungi -- and even slime molds -- survive what is rather delicately called "unfavorable conditions". When conditions improve, they sprout.

Distinctively, the sclerotium of Rhizoctonia produces no rind or internal structure, and is basically a loosely-packed clump of mycelium. These are just the sort of structures that authors Visscher, Sephton and Looy found in their end-Permian Italian rock.

So is this the smoking gun? Based on the resemblence of these fossil structures to the mature hyphae and sclerotia of modern pathogenic Rhizoctonia (the background image in this picture), the authors propose that Reduviasporonites sclerotia are "indistinguishable" from those of modern Rhizoctonia. From the presence of soilborne sclerotia, they also conclude Reduviasporonites are unlikely to have simply been wood-rotters. And previous studies have found that, in general, the more pathogenic sclerotia you find in soil, the more plant disease you find nearby. So in other words, according to the authors, finding samples of end-Permian sediments in which up to 90% of the ex-alive material in the rock is Rhizoctonia-like sclerotia as they did is like finding a smoking gun.

Modern Rhizoctonia often act as facultative pathogens. That is to say: they're opportunists. They can grow into and live relatively quietly with living trees, held in check by their immune system while waiting for them to sicken or weaken. Once they do, they attack. One of the more amazing discoveries of the last few decades is how common that is. Many plants, it seems, can have fungi living in or on them patiently waiting for a good place in line at the decay buffet. Rhizoctonia, as a pathogen, seems to stand right at the front, and would have been well-positioned to capitalize on an arboreal windfall.

Another fossilized Reduviasporonites fliament. Courtesy Cindy Looy

The authors propose the following scenario: attack by volcanic gases like carbon dioxide and methane (or whatever massive, inescapable stressor precipitated the global extinctions) weakened forests and disrupted the host-pathogen equilibrium in a way that favored the fungi, hastening the trees' already-inevitable declines. The fungi tucked in like zombies at a brains buffet.

As food dwindled and times got bad for fungi too, the massive fungal blooms went with their usual Plan B: make sclerotia. But they were storing up goods for a day that would never come. Most of their hosts were dead. No saplings could grow in the terrible conditions. Rain washed the killing fields clean, massively eroding the land, and carried the doomed sclerotia to the bottoms of watery graves, where they would be pressed into the rocks that were buried, lifted into mountains, and then finally collected by scientists who released them from their stony prisons at last. But 250 million years later, the Dinty Moore is long gone.

Let's return to the authors' original assumption, that comparing the structures of 250-million year old fossils to living creatures can help us identify them and infer what they were doing. Did the ancestors of Rhizoctonia at the dawn of the Triassic necessarily look like their descendants today? Our ancestors and the ancestors of flowering plants certainly did not.

But even if they are not genetic ancestors of modern Rhizoctonia (which the authors never claim), the fact they they seem to have evolved into the same form (as, I mentioned above, so many other unrelated fungi have done today) implies that they were doing roughly the same thing that modern Rhizoctonia and their ilk do. We call this convergent evolution, and although it would mean that you couldn't start calling Reduviasporonites "Rhizoctonia", it wouldn't change the picture the authors paint of the terrible endgame of Permian forests: global fungal apocalypse.

1In this recent study, scientists claim that the rapid buildup of CO2 could have fatally acidified the oceans, leaving marine creatures unable to build their shells.

2Rhizoctonia aren't always attacking plants; many are saprobes in soil, from which they launch their plant attacks. And the soil can be a launching place for other "deals" as well. Some can be cooperative, or "mycorrhizal" with orchids.

Tiny, nutrient-poor orchid seeds notoriously require very specific fungi to help them germinate and provide them food until they can produce their first green leaf, which may take two to 11 years (this is why growing orchids from seed outside the jungle can be, to say the least, challenging).

But, as in much of biology, all is not exactly as it seems. Though several soil fungi can colonize orchid seedlings, the Rhizoctonia (whose sexual forms are crust fungi) who can do so are also saprobes, and thus in possession of the nutrients to support a young orchid. The fungus penetrates root cortex cells and generates coils or "pelotons" in order to mediate nutrient exchange. Scientists who have watched this process have noticed that several things can happen. The seed may get colonized successfully by the appropriate fungus and grow up to be an orchid. Happy day. Or, the fungus may get out of hand and kill the seedling. Sad orchid. Finally, the fungal invasion may fail and the seedling stops growing and still dies without a fungus to launch it. This appears to be a symbiosis in the process of forming, where one false move on the part of either partner can result in death. In other words, the fungus and plant are still working out the mycorrhizal prenup. It's a delicate balance, and as with the host-pathogen equilibrium, any perturbation in the relationship can lead to disaster.

The views expressed are those of the author(s) and are not necessarily those of Scientific American.

ABOUT THE AUTHOR(S)

Jennifer Frazer

Jennifer Frazer is a AAAS Science Journalism Award-winning science writer. She has degrees in biology, plant pathology/mycology, and science writing, and has spent many happy hours studying life in situ.

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